Biogenesis of the Protein Storage Vacuole Crystalloid

Jiang, Liwen; Phillips, Thomas E.; Rogers, Sally W.; Rogers, John C.

doi:10.1083/jcb.150.4.755

Biogenesis of the Protein Storage Vacuole Crystalloid

Journal Article · Mon Aug 21 00:00:00 EDT 2000 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.150.4.755· OSTI ID:1625120

Jiang, Liwen ^[1]; Phillips, Thomas E. ^[2]; Rogers, Sally W. ^[3]; Rogers, John C. ^[3]

Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry; The Chinese Univ. of Hong Kong, Shatin, New Territories, Hong Kong (China). Dept. of Biology; DOE/OSTI
Univ. of Missouri, Columbia, MO (United States). Division of Biological Sciences
Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry

Here, we identify new organelles associated with the vacuolar system in plant cells. These organelles are defined biochemically by their internal content of three integral membrane proteins: a chimeric reporter protein that moves there directly from the ER; a specific tonoplast intrinsic protein; and a novel receptor-like RING-H2 protein that traffics through the Golgi apparatus. Highly conserved homologues of the latter are expressed in animal cells. In a developmentally regulated manner, the organelles are taken up into vacuoles where, in seed protein storage vacuoles, they form a membrane-containing crystalloid. The uptake and preservation of the contents of these organelles in vacuoles represents a unique mechanism for compartmentalization of protein and lipid for storage.

View Accepted Manuscript (DOE)

Research Organization:: Washington State Univ., Pullman, WA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC)

Grant/Contract Number:: FG03-97ER20277

OSTI ID:: 1625120

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 4 Vol. 150; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

The Zinc Finger Domain of the 43-kDa Receptor-Associated Protein, Rapsyn: Role in Acetylcholine Receptor Clustering Bezakova, Gabriela; Bloch, Robert J. Molecular and Cellular Neuroscience, Vol. 11, Issue 5-6 https://doi.org/10.1006/mcne.1998.0688	journal	August 1998
Vacuolar protein in apical and flower-petal cells Shumway, L. K.; Cheng, V.; Ryan, C. A. Planta, Vol. 106, Issue 4 https://doi.org/10.1007/bf00384766	journal	January 1972
Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue Browse, John; McCourt, Peter J.; Somerville, Christopher R. Analytical Biochemistry, Vol. 152, Issue 1 https://doi.org/10.1016/0003-2697(86)90132-6	journal	January 1986
Multivesicular bodies play a key role in vitellogenin endocytosis by Xenopus oocytes Wall, Doris A.; Patel, Sushma Developmental Biology, Vol. 119, Issue 1 https://doi.org/10.1016/0012-1606(87)90229-6	journal	January 1987
A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms Hara-Nishimura, Ikuko; Inoue, Kaori; Nishimura, Mikio FEBS Letters, Vol. 294, Issue 1-2 https://doi.org/10.1016/0014-5793(91)81349-d	journal	December 1991
Widespread occurrence of a highly conserved RING-H2 zinc finger motif in the model plant Arabidopsis thaliana Jensen, Rikke B.; Jensen, Karin L.; Jespersen, Hans M. FEBS Letters, Vol. 436, Issue 2 https://doi.org/10.1016/s0014-5793(98)01143-0	journal	October 1998
Crystal Structure of a Phosphatidylinositol 3-Phosphate-Specific Membrane-Targeting Motif, the FYVE Domain of Vps27p Misra, Saurav; Hurley, James H. Cell, Vol. 97, Issue 5 https://doi.org/10.1016/s0092-8674(00)80776-x	journal	May 1999
Plant Cells Contain Two Functionally Distinct Vacuolar Compartments Paris, Nadine; Stanley, C. Michael; Jones, Russell L. Cell, Vol. 85, Issue 4 https://doi.org/10.1016/s0092-8674(00)81256-8	journal	May 1996
Fab1p PtdIns(3)P 5-Kinase Function Essential for Protein Sorting in the Multivesicular Body Odorizzi, Greg; Babst, Markus; Emr, Scott D. Cell, Vol. 95, Issue 6 https://doi.org/10.1016/s0092-8674(00)81707-9	journal	December 1998
Vesicle transfer of storage proteins to the vacuole: The role of the Golgi apparatus and multivesicular bodies Robinson, D. G.; Bäumer, Matthias; Hinz, Giselbert Journal of Plant Physiology, Vol. 152, Issue 6 https://doi.org/10.1016/s0176-1617(98)80027-8	journal	January 1998
FYVE fingers bind PtdIns(3)P Gaullier, Jean-Michel; Simonsen, Anne; D'Arrigo, Antonello Nature, Vol. 394, Issue 6692 https://doi.org/10.1038/28767	journal	July 1998
DIP: a member of the MIP family of membrane proteins that is expressed in mature seeds and dark-grown seedlings of Antirrhinum majus Culianez-Macia, Francisco A.; Martin, Cathie The Plant Journal, Vol. 4, Issue 4 https://doi.org/10.1046/j.1365-313x.1993.04040717.x	journal	October 1993
Mutation analysis of the C-terminal vacuolar targeting peptide of tobacco chitinase: low specificity of the sorting system, and gradual transition between intracellular retention and secretion into the extracellular space Neuhaus, Jean-Marc; Pietrzak, Maciej; Boller, Thomas The Plant Journal, Vol. 5, Issue 1 https://doi.org/10.1046/j.1365-313x.1994.5010045.x	journal	January 1994
Molecular characterization of proteins in protein-body membrane that disappear most rapidly during transformation of protein bodies into vacuoles Inoue, Kaori; Motozaki, Asako; Takeuchi, Yuka The Plant Journal, Vol. 7, Issue 2 https://doi.org/10.1046/j.1365-313x.1995.7020235.x	journal	February 1995
Functional analysis of a Golgi-localized Kex2p-like protease in tobacco suspension culture cells Jiang, Liwen; Rogers, John C. The Plant Journal, Vol. 18, Issue 1 https://doi.org/10.1046/j.1365-313x.1999.00424.x	journal	April 1999
Purification and initial characterization of a potential plant vacuolar targeting receptor. Kirsch, T.; Paris, N.; Butler, J. M. Proceedings of the National Academy of Sciences, Vol. 91, Issue 8 https://doi.org/10.1073/pnas.91.8.3403	journal	April 1994
-Tonoplast intrinsic protein defines unique plant vacuole functions Jauh, G. -Y.; Fischer, A. M.; Grimes, H. D. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22 https://doi.org/10.1073/pnas.95.22.12995	journal	October 1998
Evidence for a novel route of wheat storage proteins to vacuoles. Levanony, H.; Rubin, R.; Altschuler, Y. The Journal of Cell Biology, Vol. 119, Issue 5 https://doi.org/10.1083/jcb.119.5.1117	journal	December 1992
Mannose 6-phosphate-independent targeting of lysosomal enzymes in I-cell disease B lymphoblasts. Glickman, J. N.; Kornfeld, S. Journal of Cell Biology, Vol. 123, Issue 1 https://doi.org/10.1083/jcb.123.1.99	journal	October 1993
Integral Membrane Protein Sorting to Vacuoles in Plant Cells: Evidence for Two Pathways Jiang, Liwen; Rogers, John C. The Journal of Cell Biology, Vol. 143, Issue 5 https://doi.org/10.1083/jcb.143.5.1183	journal	November 1998
A Novel RING Finger Protein Complex Essential for a Late Step in Protein Transport to the Yeast Vacuole Rieder, Stephanie E.; Emr, Scott D. Molecular Biology of the Cell, Vol. 8, Issue 11 https://doi.org/10.1091/mbc.8.11.2307	journal	November 1997
The 5[prime] Flanking Regions of Vicilin and Napin Storage Protein Genes Are Down-Regulated by Desiccation in Transgenic Tobacco Jiang, L.; Downing, W. L.; Baszczynski, C. L. Plant Physiology, Vol. 107, Issue 4 https://doi.org/10.1104/pp.107.4.1439	journal	April 1995
Molecular Cloning and Further Characterization of a Probable Plant Vacuolar Sorting Receptor Paris, N.; Rogers, S. W.; Jiang, L. Plant Physiology, Vol. 115, Issue 1 https://doi.org/10.1104/pp.115.1.29	journal	September 1997
Protein Bodies from the Endosperm of Castor Bean: Subfractionation, Protein Components, Lectins, and Changes during Germination Youle, Richard J.; Huang, Anthony H. C. Plant Physiology, Vol. 58, Issue 6 https://doi.org/10.1104/pp.58.6.703	journal	December 1976
Transport of Storage Proteins to Protein Storage Vacuoles Is Mediated by Large Precursor-Accumulating Vesicles Hara-Nishimura, Ikuko; Shimada, Tomoo; Hatano, Kyoko The Plant Cell, Vol. 10, Issue 5 https://doi.org/10.1105/tpc.10.5.825	journal	May 1998
Sorting of Phaseolin to the Vacuole Is Saturable and Requires a Short C-Terminal Peptide Frigerio, Lorenzo; de Virgilio, Maddalena; Prada, Alessandra The Plant Cell, Vol. 10, Issue 6 https://doi.org/10.1105/tpc.10.6.1031	journal	June 1998
Tonoplast Intrinsic Protein Isoforms as Markers for Vacuolar Functions Jauh, Guang-Yuh; Phillips, Thomas E.; Rogers, John C. The Plant Cell, Vol. 11, Issue 10 https://doi.org/10.1105/tpc.11.10.1867	journal	October 1999
Compartmentation of Proteins in the Endomembrane System of Plant Cells Okita, Thomas W.; Rogers, John C. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.arplant.47.1.327	journal	June 1996
Protein storage vacuoles form de novo during pea cotyledon development Hoh, B.; Hinz, G.; Jeong, B. K. Journal of Cell Science, Vol. 108, Issue 1 https://doi.org/10.1242/jcs.108.1.299	journal	January 1995
The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. F., McIntyre, G.; H., Erickson, A. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/kdgv-xe44	text	January 1993
Characterization of cis-Acting Sequences Regulating Root-Specific Gene Expression in Tobacco Yamamoto, Yuri T.; Taylor, Christopher G.; Acedo, Gregoria N. The Plant Cell, Vol. 3, Issue 4 https://doi.org/10.2307/3869212	journal	April 1991
Vacuolar Storage Proteins and the Putative Vacuolar Sorting Receptor BP-80 Exit the Golgi Apparatus of Developing Pea Cotyledons in Different Transport Vesicles Hinz, Giselbert; Hillmer, Stefan; Baumer, Matthias The Plant Cell, Vol. 11, Issue 8 https://doi.org/10.2307/3870979	journal	August 1999
Synthesis and protein body deposition of maize 15-kd zein in transgenic tobacco seeds Hoffman, Leslie M.; Donaldson, Debra D.; Bookland, Roger The EMBO Journal, Vol. 6, Issue 11 https://doi.org/10.1002/j.1460-2075.1987.tb02638.x	journal	November 1987
GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. Jefferson, R. A.; Kavanagh, T. A.; Bevan, M. W. The EMBO Journal, Vol. 6, Issue 13 https://doi.org/10.1002/j.1460-2075.1987.tb02730.x	journal	December 1987
Vacuolar protein in apical and flower-petal cells Shumway, L. K.; Cheng, V.; Ryan, C. A. Planta, Vol. 106, Issue 4 https://doi.org/10.1007/BF00384766	journal	January 1972
Correct glycosylation, Golgi-processing, and targeting to protein bodies of the vacuolar protein phytohemagglutinin in transgenic tobacco Sturm, Arnd; Voelker, Toni A.; Herman, Eliot M. Planta, Vol. 175, Issue 2 https://doi.org/10.1007/BF00392425	journal	August 1988
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms Hara-Nishimura, Ikuko; Inoue, Kaori; Nishimura, Mikio FEBS Letters, Vol. 294, Issue 1-2 https://doi.org/10.1016/0014-5793(91)81349-D	journal	December 1991
Widespread occurrence of a highly conserved RING-H2 zinc finger motif in the model plant Arabidopsis thaliana Jensen, Rikke B.; Jensen, Karin L.; Jespersen, Hans M. FEBS Letters, Vol. 436, Issue 2 https://doi.org/10.1016/S0014-5793(98)01143-0	journal	October 1998
Protein bodies, storage organelles in plant seeds Weber, E.; Neumann, D. Biochemie und Physiologie der Pflanzen, Vol. 175, Issue 4 https://doi.org/10.1016/S0015-3796(80)80070-9	journal	January 1980
Crystal Structure of a Phosphatidylinositol 3-Phosphate-Specific Membrane-Targeting Motif, the FYVE Domain of Vps27p Misra, Saurav; Hurley, James H. Cell, Vol. 97, Issue 5 https://doi.org/10.1016/S0092-8674(00)80776-X	journal	May 1999
Plant Cells Contain Two Functionally Distinct Vacuolar Compartments Paris, Nadine; Stanley, C. Michael; Jones, Russell L. Cell, Vol. 85, Issue 4 https://doi.org/10.1016/S0092-8674(00)81256-8	journal	May 1996
Fab1p PtdIns(3)P 5-Kinase Function Essential for Protein Sorting in the Multivesicular Body Odorizzi, Greg; Babst, Markus; Emr, Scott D. Cell, Vol. 95, Issue 6 https://doi.org/10.1016/S0092-8674(00)81707-9	journal	December 1998
Vesicle transfer of storage proteins to the vacuole: The role of the Golgi apparatus and multivesicular bodies Robinson, D. G.; Bäumer, Matthias; Hinz, Giselbert Journal of Plant Physiology, Vol. 152, Issue 6 https://doi.org/10.1016/S0176-1617(98)80027-8	journal	January 1998
Does this have a familiar RING? Saurin, Andrew J.; Borden, Katherine L. B.; Boddy, Michael N. Trends in Biochemical Sciences, Vol. 21, Issue 6 https://doi.org/10.1016/S0968-0004(96)80017-X	journal	June 1996
Deposition of storage proteins Müntz, Klaus Plant Molecular Biology, Vol. 38, Issue 1/2, p. 77-99 https://doi.org/10.1023/A:1006020208380	journal	January 1998
Sorting of proteins to vacuoles in plant cells Neuhaus, Jean-Marc; Rogers, John C. Plant Molecular Biology, Vol. 38, Issue 1/2, p. 127-144 https://doi.org/10.1023/A:1006032627036	journal	January 1998
A lipid associated with the antiphospholipid syndrome regulates endosome structure and function Kobayashi, Toshihide; Stang, Espen; Fang, Karen S. Nature, Vol. 392, Issue 6672 https://doi.org/10.1038/32440	journal	March 1998
DIP: a member of the MIP family of membrane proteins that is expressed in mature seeds and dark-grown seedlings of Antirrhinum majus Culianez-Macia, Francisco A.; Martin, Cathie The Plant Journal, Vol. 4, Issue 4 https://doi.org/10.1046/j.1365-313X.1993.04040717.x	journal	October 1993
Mutation analysis of the C-terminal vacuolar targeting peptide of tobacco chitinase: low specificity of the sorting system, and gradual transition between intracellular retention and secretion into the extracellular space Neuhaus, Jean-Marc; Pietrzak, Maciej; Boller, Thomas The Plant Journal, Vol. 5, Issue 1 https://doi.org/10.1046/j.1365-313X.1994.5010045.x	journal	January 1994
Molecular characterization of proteins in protein-body membrane that disappear most rapidly during transformation of protein bodies into vacuoles Inoue, Kaori; Motozaki, Asako; Takeuchi, Yuka The Plant Journal, Vol. 7, Issue 2 https://doi.org/10.1046/j.1365-313X.1995.7020235.x	journal	February 1995
Monoclonal antibodies to barley aleurain and homologs from other plants Rogers, Sally W.; Burks, Marlyn; Rogers, John C. The Plant Journal, Vol. 11, Issue 6 https://doi.org/10.1046/j.1365-313X.1997.11061359.x	journal	June 1997
Functional analysis of a Golgi-localized Kex2p-like protease in tobacco suspension culture cells Jiang, Liwen; Rogers, John C. The Plant Journal, Vol. 18, Issue 1 https://doi.org/10.1046/j.1365-313X.1999.00424.x	journal	April 1999
The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. McIntyre, G. F.; Erickson, A. H. Proceedings of the National Academy of Sciences, Vol. 90, Issue 22 https://doi.org/10.1073/pnas.90.22.10588	journal	November 1993
Identification and characterization of a RING zinc finger gene (C-RZF) expressed in chicken embryo cells. Tranque, P.; Crossin, K. L.; Cirelli, C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 7 https://doi.org/10.1073/pnas.93.7.3105	journal	April 1996
Topical aspects of vacuolar protein transport: autophagy and prevacuolar compartments Robinson, D. G.; Galili, G.; Herman, E. Journal of Experimental Botany, Vol. 49, Issue 325 https://doi.org/10.1093/jxb/49.325.1263	journal	August 1998
Accumulation of a Fusion Protein Containing 2S Albumin Induces Novel Vesicles in Vegetative Cells of Arabidopsis Hayashi, M.; Toriyama, K.; Kondo, M. Plant and Cell Physiology, Vol. 40, Issue 3 https://doi.org/10.1093/oxfordjournals.pcp.a029537	journal	January 1999
Biosynthesis and Immunolocalization of Lewis a-Containing N -Glycans in the Plant Cell Fitchette, Anne-Catherine; Cabanes-Macheteau, Marion; Marvin, Laure Plant Physiology, Vol. 121, Issue 2 https://doi.org/10.1104/pp.121.2.333	journal	October 1999
Protein Bodies of Castor Bean Endosperm: Isolation, Fractionation, and the Characterization of Protein Components Tully, Raymond E.; Beevers, Harry Plant Physiology, Vol. 58, Issue 6 https://doi.org/10.1104/pp.58.6.710	journal	December 1976
Suborganellar Localization of Proteinase Catalyzing the Limited Hydrolysis of Pumpkin Globulin Hara-Nishimura, Ikuko; Nishimura, Mikio; Matsubara, Hiroshi Plant Physiology, Vol. 70, Issue 3 https://doi.org/10.1104/pp.70.3.699	journal	September 1982
Correct Targeting of the Bean Storage Protein Phaseolin in the Seeds of Transformed Tobacco Greenwood, John S.; Chrispeels, Maarten J. Plant Physiology, Vol. 79, Issue 1 https://doi.org/10.1104/pp.79.1.65	journal	September 1985
Proglobulin Processing Enzyme in Vacuoles Isolated from Developing Pumpkin Cotyledons Hara-Nishimura, Ikuko; Nishimura, Mikio Plant Physiology, Vol. 85, Issue 2 https://doi.org/10.1104/pp.85.2.440	journal	October 1987
Protein Storage Bodies and Vacuoles Herman, Eliot M.; Larkins, Brian A. The Plant Cell, Vol. 11, Issue 4 https://doi.org/10.1105/tpc.11.4.601	journal	April 1999
Vacuolar Storage Proteins and the Putative Vacuolar Sorting Receptor BP-80 Exit the Golgi Apparatus of Developing Pea Cotyledons in Different Transport Vesicles Hinz, Giselbert; Hillmer, Stefan; Bäumer, Matthias The Plant Cell, Vol. 11, Issue 8 https://doi.org/10.1105/tpc.11.8.1509	journal	August 1999
Structural Requirements for Ligand Binding by a Probable Plant Vacuolar Sorting Receptor Cao, Xiaofeng; Rogers, Sally W.; Butler, Juliet The Plant Cell, Vol. 12, Issue 4 https://doi.org/10.1105/tpc.12.4.493	journal	April 2000
Light and electron microscope observations of a vacuolar structure associated with the floral apex of Nigella damascena Greyson, R. I.; Mitchell, K. R. Canadian Journal of Botany, Vol. 47, Issue 4 https://doi.org/10.1139/b69-085	journal	April 1969
Thin-section, freeze-fracture, and energy dispersive x-ray analysis studies of the protein bodies of tomato seeds Spitzer, Ernest; Lott, John N. A. Canadian Journal of Botany, Vol. 58, Issue 6 https://doi.org/10.1139/b80-090	journal	March 1980

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